基于序列相似性和Z曲线方法重注释原核生物蛋白编码基因

doi:10.16288/j.yczz.20-022

[an error occurred while processing this directive]

Hereditas(Beijing) ›› 2020, Vol. 42 ›› Issue (7): 691-702.doi: 10.16288/j.yczz.20-022

• Research Article • Previous Articles Next Articles

Comprehensive re-annotation of protein-coding genes for prokaryotic genomes by Z-curve and similarity-based methods

Shuo Liu¹, Zhi Zeng¹, Fancai Zeng², Mengze Du²()

^1. School of Life Science and Technology, University of Electronic Science and Technology of China, Chengdu 611731, China
^2. Department of Biochemistry and Molecular Biology, School of Basic Medicine, Southwest Medical University, Luzhou 646000,China

Received:2020-02-20 Revised:2020-05-11 Online:2020-07-20 Published:2020-06-01
Contact: Du Mengze E-mail:du_mengze@foxmail.com
Supported by:
Supported by Science Strength Improvement Plan of University of Electronic Science and Technology of China No(Y0301902610100202)

Abstract

Abstract:

The development of sequencing technology has generated huge genomic sequencing information and largely enriched public genetic resources. To analyze such big data, the algorithms and tools for comparison and annotation of genomes are updated continually, enabling genome annotation with higher accuracy via various annotation tools. Many prokaryotic genomes in public database were sequenced and assembled more than a decade ago, and they contained multiple genes with unknown functions. To improve the current annotation for those genomes in NCBI, we re-annotate 1587 bacterial and archaeal genomes using multiple prokaryotic gene recognition algorithms/softwares and gene expression data. The 33 Z-curve variables were applied to recognize sequences that were over-annotated to genes of 1587 bacterial and archaeal genomes deposited in public databases, and a total of 3092 sequences belonging to 177 genomes were recognized as sequences over-annotated as protein-coding genes. Next, 4447 protein-coding genes with unknown functions from 939 genomes were annotated with definite functions by similarity search. Finally, we recognized 2003 missed protein-coding genes that belong to known COG (clusters of orthologous groups of proteins) of nine genomes using three methods (ZCURVE 3.0, Glimmer 3.02 and Prodigal), which are accurate and frequently used for gene finding. Their algorithms are different and complementary. This is a comprehensive study for re-annotation of bacterial and archaeal genomes with new tools combining multi-omics data, which should provide a reference for annotation of newly sequenced strains, and also benefit further fundamental researches with the bacterial gene sequences obtained after re-annotation.

Key words: bacteria, re-annotation, Z-curve, hypothetical ORFs, non-coding ORFs

Shuo Liu, Zhi Zeng, Fancai Zeng, Mengze Du. Comprehensive re-annotation of protein-coding genes for prokaryotic genomes by Z-curve and similarity-based methods[J]. Hereditas(Beijing), 2020, 42(7): 691-702.

Figures/Tables 9

Fig. 1

Fig. 2

Fig. 3

Table 1

The information of genomes with recognized over-annotated ORFs of more than 20"

菌株	NC序列号	数量	菌株	NC序列号	数量
慢性型大豆根瘤菌(B. japonicum USDA 110)	NC_004463	147	金黄色葡萄球菌 (S. aureus subsp. Aureus MW2)	NC_003923	36
哈氏弧菌(Vibrio harveyi ATCC BAA-1116)	NC_009784	133	黑海甲烷袋状菌 (Methanoculleus marisnigri JR1)	NC_009051	34
大肠杆菌(E. coli CFT073)	NC_004431	119	双叶钩端螺旋体血清型Patoc菌株 (Leptospira biflexa serovar Patoc strain 'Patoc 1)	NC_010602	34
织片草螺菌 (Herbaspirillum seropedicae SmR1)	NC_014323	109	拟杆菌属 (Bacteroides salanitronis DSM 18170)	NC_015164	34
结核分枝杆菌 (Mycobacterium tuberculosis CDC1551)	NC_002755	98	巴尔通体杆菌(Bartonella clarridgeiae 73)	NC_014932	33
多形类杆菌 (Bacteroides thetaiotaomicron VPI-5482)	NC_004663	84	梅毒螺旋体梅毒亚种 (Treponema pallidum subsp. pallidum SS14)	NC_010741	32
鞘脂菌(Sphingobium japonicum UT26S)	NC_014006	80	梅毒螺旋体 (Treponema paraluiscuniculi Cuniculi A)	NC_015714	32
生丝微菌属(Hyphomicrobium sp. MC1)	NC_015717	70	鼠疫杆菌(Yersinia pestis CO92)	NC_003143	31
长双歧杆菌(B. longum NCC2705)	NC_004307	69	台湾贪铜菌 (Cupriavidus taiwanensis LMG 19424)	NC_010528	31
大肠杆菌(E. coli O157:H7 str. Sakai)	NC_002695	55	噬纤维素菌属 (Cellulophaga algicola DSM 14237)	NC_014934	31
哈维弧菌(V. harveyi ATCC BAA-1116)	NC_009783	53	结核分枝杆菌(M. tuberculosis H37Rv)	NC_000962	30
溶血葡萄球菌(S. haemolyticus JCSC1435)	NC_007168	51	沙漠自然球菌(Deinococcus deserti VCD115)	NC_012526	30
缓纤维梭菌 (Clostridium lentocellum DSM 5427)	NC_015275	51	溃疡拟杆菌(Bacteroides helcogenes P 36-108)	NC_014933	27
表皮葡萄球菌(S. epidermidis RP62A)	NC_002976	47	金黄色葡萄球菌 (S. aureus subsp. Aureus Mu50)	NC_002758	26
鼠疫杆菌(Y. pestis KIM10+)	NC_004088	46	金黄色葡萄球菌 (S. aureus subsp. Aureus N315)	NC_002745	25
海单孢菌属 (Marinomonas mediterranea MMB-1)	NC_015276	43	内脏臭气杆菌 (Odoribacter splanchnicus DSM 20712)	NC_015160	25
红球菌(Rhodococcus jostii RHA1)	NC_008268	40	嗜热盐碱细菌 (Natranaerobius thermophilus JW/NM-WN-LF)	NC_010718	23
大肠杆菌(E. coli O157:H7 str. EDL933)	NC_002655	39	圆柱杆菌(Teredinibacter turnerae T7901)	NC_012997	23
固氮密螺旋体(T. azotonutricium ZAS-9)	NC_015577	39	盐孢菌属(Salinispora tropica CNB-440)	NC_009380	20
白蚁塞巴鲁德氏菌 (Sebaldella termitidis ATCC 33386)	NC_013517	38	巴西浮霉状菌 (Planctomyces brasiliensis DSM 5305)	NC_015174	20
金黄色葡萄球菌(S. aureus subsp.COL)	NC_002951	37	苜蓿根瘤菌(Sinorhizobium meliloti AK83)	NC_015590	20
肺炎衣原体 (Chlamydophila pneumoniae AR39)	NC_002179	36

Table 1

Table 2

The information of genomes with 20 more hypothetical ORFs with annotated function"

菌株	NC序列号	数量	菌株	NC序列号	数量
大肠杆菌(E. coli O111:H-str. 11128)	NC_013364	80	炭疽芽孢杆菌(B. anthracis str. CDC 684)	NC_012581	23
肠道沙门氏菌(S. enterica subsp. enterica serovar Paratyphi B str. SPB7)	NC_010102	64	肠道沙门氏菌(S. enterica subsp. enterica serovar Paratyphi C strain RKS4594)	NC_012125	23
鲍氏志贺菌(Shigella boydii CDC 3083-94)	NC_010658	52	金黄色葡萄球菌(S. aureus subsp. aureus MW2)	NC_003923	23
肠道沙门氏菌(S. enterica subsp. arizonae serovar 62:z4, z23:- str. RSK2980)	NC_010067	45	蜡状芽孢杆菌(Bacillus cereus ATCC 10987)	NC_003909	22
枯草芽孢杆菌(B. subtilis subsp. subtilis str. 168)	NC_000964	42	大肠杆菌(E. coli O26:H11 str. 11368)	NC_013361	22
鼠李糖乳杆菌(Lactobacillus rhamnosus Lc 705)	NC_013199	38	肺炎链球菌(Streptococcus pneumoniae P1031)	NC_012467	22
鼠李糖乳杆菌(L. rhamnosus GG)	NC_013198	36	金黄色葡萄球菌(S. aureus subsp. aureus Mu3)	NC_009782	21
肠道沙门氏菌(S. enterica subsp. enterica serovar Paratyphi A str. AKU_12601)	NC_011147	35	金黄色葡萄球菌(S. aureus subsp. aureus JH9)	NC_009487	21
大肠杆菌(E. coli O157:H7 str. Sakai)	NC_002695	34	结核分枝杆菌(M. tuberculosis CDC1551)	NC_002755	20
大肠杆菌(E. coli O157:H7 str. EDL933)	NC_002655	30	炭疽芽孢杆菌(B. anthracis str. A0248)	NC_012659	20
肠道沙门氏菌(S. enterica subsp. enterica serovar Paratyphi A str. ATCC 9150)	NC_006511	30	大肠杆菌(E. coli O157:H7 str. EC4115)	NC_011353	20
大肠杆菌(E. coli SE11)	NC_011415	28	炭疽芽孢杆菌(B. anthracis str. Ames)	NC_003997	20
大肠杆菌(E. coli ED1a)	NC_011745	27	哈维氏弧菌(V. harveyi ATCC BAA-1116)	NC_009783	20
大肠杆菌(E. coli UTI89)	NC_007946	26	结核分枝杆菌(M. tuberculosis KZN 1435)	NC_012943	20
枯草芽孢杆菌(B. subtilis BSn5)	NC_014976	25	大肠杆菌(E. coli O55:H7 str. CB9615)	NC_013941	20
肠道沙门氏菌 (S. enterica subsp. enterica serovar Typhi str. Ty2)	NC_004631	25	牛型分枝杆菌 (Mycobacterium bovis AF2122/97)	NC_002945	20
大肠杆菌(E. coli CFT073)	NC_004431	23

Table 2

Table 3

Table 4

Fig. 4

Supplementary Fig. 1

References 43

[1]	Mørk S, Holmes I . Evaluating bacterial gene-finding HMM structures as probabilistic logic programs. Bioinformatics, 2012,28(5):636-642.
[2]	Warren AS, Archuleta J, Feng WC, Setubal JC . Missing genes in the annotation of prokaryotic genomes. BMC Bioinformatics, 2010,11(1):131.
[3]	Salzberg SL . Next-generation genome annotation: we still struggle to get it right. Genome Biol, 2019,20(1):92.
[4]	Breitwieser FP, Pertea M, Zimin AV, Salzberg SL . Human contamination in bacterial genomes has created thousands of spurious proteins. Genome Res, 2019,29(6):954-960.
[5]	Fleischmann RD, Adams MD, White O, Clayton RA, Kirkness EF, Kerlavage AR, Bult CJ, Tomb JF, Dougherty BA, Merrick JM, Mckenney K, Sutton G, FitzHugh W,Fields C,Gocayne JD,Scott J,Shirley R,Liu LL,Glodek A,Kelley JM,Weidman JF,Phillips CA,Spriggs T,Hedblom E,Cotton MD,Utterback TR,Hanna MC,Nguyen DT,Saudek DM,Brandon RC,Fine LD,Fritchman JL,Fuhrmann JL,Geoghagen NSM,Gnehm CL,McDonald LA,Small KV,Fraser CM,Smith HO,Venter JC. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science, 1995,269(5223):496-512.
[6]	Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW . Genbank. Nucleic Acids Res, 2009,37(Database issue):D26-D31.
[7]	Yu JF, Xiao K, Jiang DK, Guo J, Wang JH, Sun X . An Integrative method for identifying the over-annotated protein-coding genes in microbial genomes. DNA Res, 2011,18(6):435-449.
[8]	Hua ZG, Lin Y, Yuan YZ, Yang DC, Wei W, Guo FB . ZCURVE 3.0: identify prokaryotic genes with higher accuracy as well as automatically and accurately select essential genes. Nucleic Acids Res, 2015,43(W1):W85-W90.
[9]	Zickmann F, Renard BY . IPred-integrating ab initio and evidence based gene predictions to improve prediction accuracy. BMC Genomics, 2015,16(1):134.
[10]	Keilwagen J, Wenk M, Erickson JL, Schattat MH, Grau J, Hartung F . Using intron position conservation for homology-based gene prediction. Nucleic Acids Res, 2016,44(9):e89.
[11]	Besemer J, Lomsadze A, Borodovsky M . GeneMarkS:a self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions. Nucleic Acids Res, 2001,29(12):2607-2618.
[12]	Kelley DR, Liu B, Delcher AL, Pop M, Salzberg SL . Gene prediction with Glimmer for metagenomic sequences augmented by classification and clustering. Nucleic Acids Res, 2012,40(1):e9.
[13]	Larsen TS, Krogh A . EasyGene-a prokaryotic gene finder that ranks ORFs by statistical significance. BMC Bioinformatics, 2003,4(1):21.
[14]	Guo FB, Ou HY, Zhang CT . ZCURVE: a new system for recognizing protein-coding genes in bacterial and archaeal genomes. Nucleic Acids Res, 2003,31(6):1780-1789.
[15]	Du MZ, Guo FB, Chen YY . Gene re-annotation in genome of the extremophile Pyrobaculum Aerophilum by using bioinformatics methods. J Biomol Struct Dyn, 2011,29(2):391-401.
[16]	Guo FB, Xiong LF, Teng JL, Yuen KY, Lau SK, Woo PC . Re-annotation of protein-coding genes in 10 complete genomes of Neisseriaceae family by combining similarity- based and composition-based methods. DNA Res, 2013,20(3):273-286.
[17]	Lei Y, Kang SK, Gao JX, Jia XS, Chen LL . Improved annotation of a plant pathogen genome Xanthomonas oryzae pv. oryzae PXO99A. J Biomol Struct Dyn, 2013,31(3):342-350.
[18]	Mao Y, Yang X, Liu Y, Yan Y, Du Z, Han Y, Song Y, Zhou L, Cui Y, Yang R . Reannotation of Yersinia pestis strain 91001 Based on Omics Data. Am J Trop Med Hyg, 2016,95(3):562-570.
[19]	Pfeiffer F, Bagyan I, Alfaro‐Espinoza G,Zamora‐Lagos MA,Habermann B,Marin‐Sanguino A,Oesterhelt D,Kunte HJ. Revision and reannotation of the Halomonas elongata DSM 2581T genome. MicrobiologyOpen, 2017,6(4):e00465.
[20]	Delcher AL, Bratke KA, Powers EC, Salzberg SL . Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics, 2007,23(6):673-679.
[21]	Zhang R, Zhang CT . A Brief Review:The Z-curve theory and its application in genome analysis. Curr Genomics, 2014,15(2):78-94.
[22]	Weiss MC, Sousa FL, Mrnjavac N, Neukirchen S, Roettger M, Nelson-Sathi S, Martin WF . The physiology and habitat of the last universal common ancestor. Nat Microbiol, 2016,1(9):16116.
[23]	Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW, Hauser LJ . Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics, 2010,11(1):119.
[24]	Barrett TT, Troup DB, Wilhite SE, Ledoux P, Rudnev D, Evangelista C, Kim IF, Soboleva A, Tomashevsky M, Marshall KA, Phillippy KH, Sherman PM, Muertter RN, Edgar R . NCBI GEO: archive for high-throughput functional genomic data. Nucleic Acids Res, 2009,37(Database issue):D885-D890.
[25]	Wang M, Weiss M, Simonovic M, Haertinger G, Schrimpf SP, Hengartner MO,von Mering C. PaxDb, a database of protein abundance averages across all three domains of life. Mol Cell Proteomics, 2012,11(8):492-500.
[26]	McGinnis S, Madden TL . BLAST: at the core of a powerful and diverse set of sequence analysis tools. Nuleic Acids Res, 2004,32(Suppl.2):W20-W25.
[27]	Wood DE, Lin H, Levy-Moonshine A, Swaminathan R, Chang YC, Anton BP, Osmani L, Steffen M, Kasif S, Salzberg SL . Thousands of missed genes found in bacterial genomes and their analysis with COMBREX. Biol Direct, 2012,7(1):37.
[28]	Huerta-Cepas J, Szklarczyk D, Forslund K, Cook H, Heller D, Walker MC, Rattei T, Mende DR, Sunagawa S, Kuhn M, Jensen LJ, Mering CV, Bork P. eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences. Nucleic Acids Res, 2016,44(Database issue):D286-D293.
[29]	Wu ST, Zhu ZW, Fu LM, Niu BF, Li WZ . WebMGA: a customizable web server for fast metagenomic sequence analysis. BMC Genomics, 2011,12(1):444.
[30]	Tatusov RL, Galperin MY, Natale DA, Koonin EV . The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res, 2000,28(1):33-36.
[31]	Qi J, Luo H, Hao BL . CVTree: a phylogenetic tree reconstruction tool based on whole genomes. Nucleic Acids Res, 2004,32:W45-W47.
[32]	Hockenbery D, Nuñez G, Milliman C, Schreiber RD, Korsmeyer SJ . Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature, 1990,348(6299):334-336.
[33]	Liu WQ, Feng Y, Wang Y, Zou QH, Chen F, Guo JT, Peng YH, Jin Y, Li YG, Hu SN, Johnson RN, Liu GR, Liu SL . Salmonella paratyphi C: Genetic divergence from Salmonella choleraesuis and pathogenic convergence with Salmonella typhi. PLoS One, 2009,4(2):e4510.
[34]	Vankuren NW, Long M . Gene duplicates resolving sexual conflict rapidly evolved essential gametogenesis functions. Nat Ecol Evol, 2018,2(4):705-712.
[35]	Minor LL, Bockemühl J . 1987 supplement (no.31) to the schema of Kauffmann-White. Ann Inst Pasteur Microbiol, 1988,139(3):331-335.
[36]	Dwyer DJ, Belenky PA, Yang JH, Macdonald IC, Martell JD, Takahashi N, Chan CT,lobritz MA,Braff D,Schwarz EG,Ye JD,Pati M,Vercruysse M,Ralifo PS,Allison KR,Khalil AS,Ting AY,Walker GC,Collins JJ. Antibiotics induce redox-related physiological alterations as part of their lethality. Proc Natl Acad Sci USA, 2014,111(20):E2100-E2109.
[37]	Hadjeras L, Poljak L, Bouvier M, Morin-Ogier Q, Canal l,Cocaign-Bousquet M,Girbal L,Carpousis AJ. Detachment of the RNA degradosome from the inner membrane of Escherichia coli results in a global slowdown of mRNA degradation, proteolysis of RNase E and increased turnover of ribosome-free transcripts. Mol Microbiol, 2019,111(6):1715-1731.
[38]	Kim S, Yu Z, Kil RM, Lee M . Deep learning of support vector machines with class probability output networks. Neural Netw, 2015,64:19-28.
[39]	Guo FB . The distribution patterns of bases of protein- coding genes, non-coding ORFs, and intergenic sequences in Pseudomonas aeruginosa PA01 genome and its implication. J Biomol Struct Dyn, 2007,25(2):127-133.
[40]	Uyar B, Yusuf D, Wurmus R, Rajewsky N, Ohler U, Akalin A . RCAS: an RNA centric annotation system for transcriptome-wide regions of interest. Nucleic Acids Res, 2017,45(10):e91.
[41]	Huang Y, Liu Q, Chi LJ, Shi CM, Wu Z, Hu M, Shi H, Chen H . Application of BIG-Annotator in the genome sequencing data functional annotation and genetic diagnosis. Hereditas(Beijing), 2018,40(11):1015-1023.
	黄莹, 刘琪, 池连江, 石承民, 吴祯, 胡敏, 石宏, 陈华 . BIG-Annotator: 基因组测序数据高效功能注释及其在遗传诊断中的应用. 遗传, 2018,40(11):1015-1023.
[42]	Bick JT, Zeng SQ, Robinson MD, Ulbrich SE, Bauersachs S . Mammalian Annotation Database for improved annotation and functional classification of Omics datasets from less well-annotated organisms. Database(Oxford), 2019,2019:1-16.
[43]	Ravindran SP, Lüneburg J, Gottschlich L, Tams V, Cordellier M . Daphnia stressor database: Taking advantage of a decade of Daphnia ‘-omics’ data for gene annotation. Sci Rep, 2019,9(1):11135.

Metrics

Comments

www.chinagene.cn
备案号：京ICP备09063187号

正/负链(在基因组上位置)	同源序列来源	功能	E值	覆盖度 (%)	一致性 (%)
负链(190551~191603)	肠道沙门菌 (S. enterica subsp. enterica)	亮氨酸操纵子先导肽 (leu operon leader peptide)	8e-139	79	74.01
负链(2228549~2228758)	志贺氏菌属(Shigella)	多药耐药外膜蛋白MdtQ (multidrug resistance outer membrane protein MdtQ)	1e-27	72	100
负链(4322661~4323281)	志贺氏菌属(Shigella)	Pn转运体膜通道蛋白组分(membrane channel protein component of Pn transporter)	4e-108	77	98.74
负链(4500432~4500791)	猪布鲁氏杆菌(Brucella suis)	磷酸乙醇胺转移酶(MULTISPECIES: phosphoethanolamine transferase)	3e-45	69	91.57
正链(1465410~1467950)	宋内志贺菌(Shigella sonnei)	包含蛋白质的自转运体结构域 (autotransporter domain-containing protein)	0.0	74	87.03
正链(1470858~1474013)	福氏志贺氏菌 (Shigella flexneri)	自转运体外膜β管(MULTISPECIES: autotransporter outer membrane beta-barrel)	0.0	76	100
正链(2070501~2071211)	双歧杆菌 (Bifidobacterium longum)	GTPase家族蛋白(GTPase family protein)	4e-129	77	99.45
正链(3993850~3994335)	痢疾志贺氏菌 (Shigella dysenteriae 1617)	CyaX蛋白(CyaX protein)	9e-67	63	96.12
负链(4506626~4506883)	红树杆菌属 (Mangrovibacter plantisponsor)	表皮粘着蛋白E (surface-adhesin protein E)	1e-28	98	60

菌株	NC序列号	基因组大小(bp)	基因总数	新基因的数目
枯草芽孢杆菌(B. subtilis subsp. subtilis str. 168)	NC_000964	4215606	4175	52
金黄色葡萄球菌(S. aureus subsp. aureus NCTC 8325)	NC_007795	2821361	2767	61
酿脓链球菌(S. pyogenes SF370)	NC_002737	1852441	1696	104
流感嗜血杆菌(H. influenzae Rd KW20)	NC_000907	1830138	1610	123
嗜酸氧化亚铁硫杆菌(A. ferrooxidans ATCC 23270)	NC_011761	2982397	3147	143
大肠杆菌(E. coli str. K-12 substr. MG1655)	NC_000913	4641652	4140	246
脑膜炎奈瑟球菌(N. meningitidis MC58)	NC_003112	2272360	1953	279
炭疽芽孢杆菌(B. anthracis str. Ames)	NC_003997	5227293	5039	418
肠道沙门氏菌(S. enterica subsp. enterica serovar Typhi str. CT18)	NC_003198	4809037	4111	577

Comprehensive re-annotation of protein-coding genes for prokaryotic genomes by Z-curve and similarity-based methods

RichHTML

PDF (PC)

Knowledge

Abstract

Cite this article

share this article

Figures/Tables 9

References 43

Related Articles 15

Recommended Articles

Metrics

Comments

[1]	Zhongling Wen, Minkai Yang, Xingyu Chen, Chenyu Hao, Ran Ren, Shujuan Chu, Hongwei Han, Hongyan Lin, Guihua Lu, Jinliang Qi, Yonghua Yang. Bacterial composition, function and the enrichment of plant growth promoting rhizobacteria (PGPR) in differential rhizosphere compartments of Al-tolerant soybean in acidic soil [J]. Hereditas(Beijing), 2021, 43(5): 487-500.
[2]	Jinyu Li, Shan Yang, Yujun Cui, Tao Wang, Yue Teng. Research progress of bacterial minimal genome [J]. Hereditas(Beijing), 2021, 43(2): 142-159.
[3]	Chao Yang, Ruifu Yang, Yujun Cui. Bacterial genome-wide association study: methodologies and applications [J]. Hereditas(Beijing), 2018, 40(1): 57-65.
[4]	Lingxian Yi,Yiyun Liu,Renjie Wu,Zisen Liang,Jian-Hua Liu. Research progress on the plasmid-mediated colistin resistance gene mcr-1 [J]. Hereditas(Beijing), 2017, 39(2): 110-126.
[5]	Xiaonan Pang, Xiao Hong, Xuan Wei, Xiwen Chen, Jia Liu, Defu Chen. Research progress in physicochemical characteristics of lactoferrin and its recombinant expression systems [J]. HEREDITAS(Beijing), 2015, 37(9): 873-884.
[6]	Zhifang Li, Zili Feng, Lihong Zhao, Yongqiang Shi, Hongjie Feng, Heqin Zhu. Effects of transgenic cotton expressing chitinase and glucanase genes on the diversity of soil bacterial community [J]. HEREDITAS(Beijing), 2015, 37(8): 821-827.
[7]	Longxiang Xie, Zhaoxiao Yu, Siyao Guo, Ping Li, Abualgasim Elgaili Abdalla, Jianping Xie. The roles of epigenetics and protein post-translational modifications in bacterial antibiotic resistance [J]. HEREDITAS(Beijing), 2015, 37(8): 793-800.
[8]	Kai Xia, Xinle Liang, Yudong Li. Comparative genomics and evolutionary analysis of CRISPR loci in acetic acid bacteria [J]. HEREDITAS(Beijing), 2015, 37(12): 1242-1250.
[9]	YANG Xiao-Liang, BAI Da-Zhang, QIU Wei, DONG Hui-Qin, LI Da-Quan, CHEN Fang, MA Run-Lin, Hugh T Blair, GAO Jian-Feng. Screening of tissues pooled cDNA library using probes by restricted fragments of BAC positive clones of ovine MHC [J]. HEREDITAS, 2012, 34(7): 887-894.
[10]	XIAO Feng, LI Ren-Hui. Cyanobacterial genome transposable element mining and analysis based on 454 deep-sequencing data set [J]. HEREDITAS, 2011, 33(6): 654-660.
[11]	BANG Wen-Fang, LV Jian-Wei, LIN Xiao-Beng, HUANG Chi, DIAO Xin-Yan, WEN Ai-Gen, JIANG Hui-Fang. Differential expression of genes related to bacterial wilt resistance in peanut (Arachis hypogaea L.) [J]. HEREDITAS, 2011, 33(4): 389-396.
[12]	XIE Che-Chu, GU Hai-Yun, CHEN Ru-Hua. Regulation of chitinase genes expression in bacteria [J]. HEREDITAS, 2011, 33(10): 1029-1038.
[13]	XIE Zhao-Hui. The roles of RNA silencing in plant biotic stress [J]. HEREDITAS, 2010, 32(6): 561-570.
[14]	ZHANG Ju-Yong, HUANG Cheng-Feng, WANG Wei, XU An-Long, WANG Xi-Quan. Construction of genome BAC library for single Branchiostoma belcheri individual [J]. HEREDITAS, 2010, 32(1): 67-72.
[15]	REN Hong-Lin, XU Dan-Dan, QIAO Kun, CAI Ling, HUANG Wei-Bin, ZHANG Nai, WANG Ke-Jian. Construction of SSH library from haemocyte of variously colored abalone challenged with bacteria and differential expression analysis of macrophage expressed protein [J]. HEREDITAS, 2008, 30(8): 1043-1050.